Primula nutans

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Trophic mode

Parasitism and mycoheterotrophy: autotroph

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Parasitism and mycoheterotrophy
In plant parasitism, two groups can be distinguished based on two different mechanisms. The first group of parasitic plants includes those directly parasitizing on another plant. These plants are called haustorial parasites. Using a specialized organ, the haustorium, they attach themselves to other plants and uptake resources from the host’s vascular bundles. The second group comprises mycoheterotrophic plants, which parasitise fungi via mycorrhizal interactions and gain organic carbon from them. Plants in both groups display variable dependence on their host organism.

The functional categorization of parasitic plants has been a topic of an active debate that is still ongoing. The traditional categories are based on the ability to perform photosynthesis (photosynthetic hemiparasites and non-green holoparasites) and the location of the haustoria (root and stem parasites) (Heide-Jørgensen 2008). However, such a classification system struggles with phenomena such as rudimentary photosynthesis in some species, variable photosynthetic activity throughout the life cycle, and the existence of parasitic plants that integrate with their host to such an extent that they can be considered endophytic. For the functional classification of European parasitic plants, we have adopted the most recent classification system proposed by Teixeira-Costa & Davis (2021) with small further modifications. This system relies primarily on ontogenetic development and strategies of attachment to the host. The values of other important functional traits, including photosynthetic capacity, type of vascular bundle connection, development of the primary haustorium, and location of haustoria on the host are also well discriminated by the categories of Teixeira-Costa & Davis (2021).

Euphytoid hemiparasites represent a great majority of European parasitic plants. These are root-parasitic, photosynthetic plants that germinate independently of the presence of the host and produce exclusively lateral (secondary) haustoria with a vascular connection to the host xylem only. All European species belong to the Orobanchaceae and Santalaceae. Teixeira-Costa & Davis (2021) call these plants “euphytoid parasites”, but we prefer keeping “hemiparasites” in the name of this category to preserve this well-established term.

Obligate root parasites comprise all species of non-green root holoparasites (such as Orobanche spp.), but also hemiparasitic species, which are more dependent on their host than the euphytoid hemiparasites due to the absence of photosynthesis in the initial life stage (e.g. Striga spp.). Most of them produce terminal (primary) haustoria immediately after seed germination, triggered by chemical cues of host presence. However, several European obligate root parasites (holoparasitic Lathraea spp., hemiparasitic Tozzia alpina, and perennial species of Rhynchocorys) deviate from this developmental pattern by germinating without host cues and not forming primary haustoria (Těšitel 2016).

Mistletoes are epiphytic parasitic shrubs. They germinate on host stems or branches and penetrate the host with a primary haustorium. The level of photosynthesis varies among the mistletoe species from efficient to rudimentary. The most widespread mistletoes of Loranthus and Viscum display efficient photosynthesis. By contrast, the Mediterranean genus Arceuthobium connects to the host’s phloem and takes up substantial amounts of carbon from the host (Rey et al. 1991). The photosynthetic capacity of Arceuthobium is probably limited, as shown by physiological data from their American congeners (Miller & Tocher 1975).

Parasitic vines are herbaceous parasites that attach themselves to the stems of their hosts by haustoria that are formed on the parasite stem. They germinate on the soil surface and, during a period of independent growth, forage for a host to which they attach themselves with lateral haustoria. All European parasitic vines belong to the genus Cuscuta and have only rudimentary photosynthesis, which however has an important function in seedling metabolism and seed production (McNeal et al. 2007).

Endophytic parasites (or Endoparasites) are the most integrated with the host body among parasitic plants. They are rootless, stemless and leafless, grow most of their life as filaments within their host and are only visible outside the host body when flowering. The holoparasitic Cytinus hypocistis and Pilostyles haussknechtii are the only species of this category in the European flora.

In mycoheterotrophic plants, the initial developmental stages (gametophytes in lycophytes and ferns or belowground seedling stages of other plants) are not green, obtaining all their organic carbon and other resources from the fungus. The adult stages are still dependent on the mycorrhizal fungi as a source of water and mineral nutrients but vary in their dependence on heterotrophic carbon: there is a continuum from autotrophy, where the adult plants no longer use fungal carbon (this strategy is further called ‘initial mycoheterotrophy’), through mixotrophy (the adult plants combine autotrophic with heterotrophic nutrition; further called ‘partial mycoheterotrophy’), to heterotrophy (further called ‘full mycoheterotrophy’) (Merckx 2012). Two categories are distinguished here:

Initial and partial mycoheterotrophs have been combined here into a common category because the level of carbon heterotrophy may be low or depend on light conditions (Preiss et al. 2010), which makes it difficult to distinguish between partial mycoheterotrophs and initial mycoheterotrophs. Furthermore, new partially mycoheterotrophic species may be identified due to the advancement of the stable-isotope methodology (e.g., Schiebold et al. 2018). This category includes mycoheterotrophic species from Ophioglossaceae, Lycopodiaceae, green mycoheterotrophic species from Ericaceae (subfamily Pyroloideae) and all green Orchidaceae. Species that obtain nearly all of their carbon from mycorrhizal fungi but still contain chlorophyll and can be photosynthetically active, such as Corallorhiza trifida (Zimmer et al. 2008, Cameron et al. 2009) and Limodorum species (Bellino et al. 2014) from Orchidaceae, are also included in this category. Interestingly, achlorophyllous individuals, which completely lack chlorophyll and wholly depend on their mycorrhizal fungi, are rarely found among partially mycoheterotrophic species (e.g., in the genera Cephalanthera and Epipactis).

Full mycoheterotrophs include achlorophyllous species that cannot photosynthesize and obtain carbon only from mycorrhizal fungi during their life cycle. Neottia nidus-avis and Epipogium aphyllum from Orchidaceae and Hypopitys monotropa and H. hypophegea from Ericaceae are the only species in this category in the European flora.

Categories

autotroph

euphytoid hemiparasite

obligate root parasite

mistletoe

parasitic vine

endophytic parasite

initial or partial mycoheterotroph

full mycoheterotroph

Data source and citation

Těšitel, J., Těšitelová, T., Fahs, N., Blažek, P., Knotková, K. & Axmanová, I. (2024): Parasitism and mycoheterotrophy. – www.FloraVeg.eu.

Further references

Bellino, A., Alfani, A., Selosse, M.-A., Guerrieri, R., Borghetti, M., & Baldantoni, D. (2014). Nutritional regulation in mixotrophic plants: New insights from Limodorum abortivum. Oecologia, 175(3), 875–885. https://doi.org/10.1007/s00442-014-2940-8
Cameron, D. D., Preiss, K., Gebauer, G., & Read, D. J. (2009). The chlorophyll-containing orchid Corallorhiza trifida derives little carbon through photosynthesis. New Phytologist, 183(2), 358–364. https://doi.org/10.1111/j.1469-8137.2009.02853.x
Heide-Jørgensen, H. S. (2008). Parasitic flowering plants. Brill, Leiden.
Kubat, R. & Weber, H. C. (1987). Zur Biologie von Rhynchcorys elephas (L.) Griseb. (Scrophulariaceae). Beiträge zur Biologie der Pflanzen, 62, 239–250.
McNeal, J. R., Arumugunathan, K., Kuehl, J. V., Boore, J. L., & dePamphilis, C. W. (2007). Systematics and plastid genome evolution of the cryptically photosynthetic parasitic plant genus Cuscuta (Convolvulaceae). BMC Biology, 5(1), 55. https://doi.org/10.1186/1741-7007-5-55
Merckx, V. S. F. T. (Ed). (2012). Mycoheterotrophy: the biology of plants living on fungi. Springer, Berlin.
Miller, J. R., & Tocher, R. D. (1975). Photosynthesis and respiration of Arceuthobium tsugense (Loranthaceae). American Journal of Botany, 62(7), 765–769. https://doi.org/10.2307/2442068
Preiss, K., Adam, I. K. U., & Gebauer, G. (2010). Irradiance governs exploitation of fungi: Fine-tuning of carbon gain by two partially myco-heterotrophic orchids. Proceedings of the Royal Society B: Biological Sciences, 277(1686), 1333–1336. https://doi.org/10.1098/rspb.2009.1966
Rey, L., Sadik, A., Fer, A., & Renaudin, S. (1991). Trophic relations of the dwarf mistletoe Arceuthobium oxycedri with its host Juniperus oxycedrus. Journal of Plant Physiology, 138(4), 411–416. https://doi.org/10.1016/S0176-1617(11)80515-8
Schiebold, J. M.-I., Bidartondo, M. I., Lenhard, F., Makiola, A., & Gebauer, G. (2018). Exploiting mycorrhizas in broad daylight: Partial mycoheterotrophy is a common nutritional strategy in meadow orchids. Journal of Ecology, 106(1), 168–178. https://doi.org/10.1111/1365-2745.12831
Teixeira-Costa, L., & Davis, C. C. (2021). Life history, diversity, and distribution in parasitic flowering plants. Plant Physiology, 187(1), 32–51. https://doi.org/10.1093/plphys/kiab279
Těšitel, J. (2016). Functional biology of parasitic plants: A review. Plant Ecology and Evolution, 149(1), Article 1. https://doi.org/10.5091/plecevo.2016.1097
Těšitel, J., Těšitelová, T., Blažek, P., & Lepš, J. (2016). Parasitism and mycoheterotrophy. www.pladias.cz.
Weber, H. C. (1973). Zur Biologie von Tozzia alpina L. (Standort, Wirtspflanzen, Entwicklung und Parasitismus). Beiträge zur Biologie der Pflanzen, 49, 237–249.
Zimmer, K., Meyer, C., & Gebauer, G. (2008). The ectomycorrhizal specialist orchid Corallorhiza trifida is a partial myco-heterotroph. New Phytologist, 178(2), 395–400. https://doi.org/10.1111/j.1469-8137.2007.02362.x
Carnivory: non-carnivorous

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Carnivory
Carnivorous plants attract, trap and kill their prey, mainly insects, small crustaceans and protozoans, and subsequently absorb the nutrients from the dead bodies. Carnivorous species occur in environments with extremely low availability of nutrients, especially nitrogen and phosphorus, e.g. mires. In contrast, they usually have enough light (open habitats) and high water table or precipitation levels (Fleischmann et al. 2017). Therefore, the carnivory improves the intake of nutrients essential for growth but sparse in the environment, while the main source of energy for these plants is photosynthesis (Fleischmann et al. 2017).

Although there is a variety of morphological structures and trapping mechanisms, all the traps evolved as more or less complicated modifications of leaves with glandulous hairs (Hedrich & Fukushima 2021). Examples of active-hunting carnivorous plants include Aldrovanda with snap traps and Utricularia with suction traps. Typical representatives of the passive-trapping species can be found in the genera Drosera, Drosophyllum and Pinguicula, which have specific types of adhesive leaves. Another passive mechanism is the pitfall trap of Sarracenia (Hedrich & Fukushima 2021). Some species can combine adhesive traps with active movement of either glands or parts of the leaves (e.g. some species of Drosera).

The carnivory evolved independently in relatively distant lineages of angiosperms. There are carnivorous families within the orders Poales, Oxalidales, Caryophyllales, Ericales and Lamiales (Hedrich & Fukushima 2021). This convergent evolution of carnivory was possible because the traits associated with carnivorous syndrome from trap development through prey digestion to nutrient absorption are modifications of structures found also in non-carnivorous ancestors, where these originally served as defending mechanisms (Hedrich & Fukushima 2021).

In Europe, there are only three native carnivorous families, namely Droseraceae, Drosophyllaceae (order Caryophyllales), and Lentibulariaceae (Lamiales). Carnivorous plants have however often been planted and imported to Europe. Some of these non-native carnivorous species introduced to Europe can also survive in natural habitats and establish vital populations. For example, the species of Sarracenia (Sarraceniaceae, Ericales), native to North America, have nowadays scattered secondary occurrences across western and northwestern Europe.

Categories

carnivorous

non-carnivorous

Data source and citation

Axmanová, I. (2023): Carnivory. – www.FloraVeg.eu.

Further references

Fleischmann, A., Schlauer, J., Smith, S. A., & Givnish, T. J. (2017). Evolution of carnivory in angiosperms. In Ellison, A. & Adamec, L. (Eds.), Carnivorous Plants: Physiology, ecology, and evolution (p. 22–41). Oxford University Press. https://doi.org/10.1093/oso/9780198779841.003.0003
Hedrich, R., & Fukushima, K. (2021). On the Origin of Carnivory: Molecular Physiology and Evolution of Plants on an Animal Diet. Annual Review of Plant Biology, 72(1), 133–153. https://doi.org/10.1146/annurev-arplant-080620-010429
Symbiotic nitrogen fixation: no nitrogen-fixing symbionts

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Symbiotic nitrogen fixation
Plants that are able to form a symbiosis with nitrogen-fixing bacteria are classified as nitrogen-fixing plants or nitrogen fixers. Specific bacteria are able to fix atmospheric nitrogen in a way to make it directly accessible to the plants (Franche et al. 2009). For providing nitrogen to the plant, the bacteria receive carbon in return (Crews, 1999, Dilworth et al., 2008). When forming a symbiosis with vascular plants, these bacteria usually inhabit the roots of their symbiont, forming so called (root-)nodules (Akkermans & Houwers, 1983, Fyson & Sprent, 1980, Loureiro et al., 1994). Three different symbiotic relationships between vascular plants and bacteria can be distinguished: (1) with the endosymbiotic cyanobacteria Nostoc, (2) with rhizobia (e.g. Allorhizobium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium) and (3) with Frankia, so-called actinorhizal plants (Bond 1983, Pawlowski & Sprent 2007, Sprent 2008, Benson 2016, Tedersoo et al., 2018). Nitrogen fixation is not a completely phylogenetically conserved trait but evolved and disappeared a few times in the evolution of plants. For the first time it evolved in the Cycadales in Gymnosperms (symbiosis with cyanobacteria, plant species not native to Europe). Most of the nitrogen-fixing plants are however phylogenetically related and recruit from the so-called “Nitrogen-fixing clade” sensu Soltis et al. (1995). Only the family Zygophyllaceae (associated with rhizobia) and the non-native Gunnera, the only genus recorded in Europe associated with Nostoc, do not belong to this clade, representing the exceptions in Angiosperms. Only five native taxa (the genus Alnus, Hippophae rhamnoides, Myrica gale, Elaeagnus angustifolia and Coriaria myrtifolia) and some non-native species with sporadic occurrence are associated with Frankia in Europe. The largest number of nitrogen-fixing species form symbiosis with rhizobia. This includes almost all Fabaceae (uncertain genera and likely exceptions, respectively, are known only very few occurring in Europe: among others this includes Cercis, Erinacea, Gonocytisus, Hammatolobium, Podocytisus, Dorycnopsis (all native), Gleditsia, Cytisopsis, Styphnolobium, Gymnocladus (not native), plus Zygophyllaceae (with uncertain genera Balanites, Seetzenia and Tetraena occurring in Europe).

Assignment was done on the genus-level. Although rare cases of species-specific differences concerning the symbiotic nitrogen fixation status within one genus are known worldwide, for the European flora the general consent that the status is conserved on the genus level is still accepted. Assignment of “likely” or “unlikely” symbiosis with rhizobia is mainly based on their phylogenetic position where there has been no scientific study investigating the nitrogen fixation status of the genus directly or if studies showed diverging results.

Categories

symbiosis with rhizobia

likely symbiosis with rhizobia

unlikely symbiosis with rhizobia

symbiosis with frankia

symbiosis with cyanobacteria

no nitrogen-fixing symbionts

Data source and citation

Fahs, N., Blažek, P., Těšitel, J. & Axmanová, I. (2023). Symbiotic nitrogen fixation. – www.FloraVeg.eu.

Further references

Benson D. R. (2016). Frankia & actinorhizal plants. Available at https://frankia.mcb.uconn.edu/ [accessed on 1 Feb 2021]
Blažek, P. & Lepš, J. (2016). Symbiotic nitrogen fixation. – www.pladias.cz.
Bond, G. (1983). Taxonomy and distribution of non-legume nitrogen-fixing systems. In J. C. Gordon & C. T. Wheeler (Eds.), Biological nitrogen fixation in forest ecosystems: Foundations and applications (pp. 55–87). Springer Netherlands. https://doi.org/10.1007/978-94-009-6878-3_3
Crews, T. E. (1999). The presence of nitrogen fixing legumes in terrestrial communities: Evolutionary vs ecological considerations. Biogeochemistry, 46(1), 233–246. https://doi.org/10.1007/BF01007581
Dilworth M. J., James E. K., Sprent J. I., & Newton W. E. (Eds). (2008). Nitrogen-Fixing Leguminous Symbioses. Springer Netherlands.
Franche, C., Lindström, K., & Elmerich, C. (2009). Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant and Soil, 321(1), 35–59. https://doi.org/10.1007/s11104-008-9833-8
Fyson, A., & Sprent, J. I. (1980). A Light and Scanning Electron Microscope Study of Stem Nodules in Vicia faba L. Journal of Experimental Botany, 31(123), 1101–1106.
Loureiro, M. F., DE Faria, S. M., James, E. K., Pott, A., & Franco, A. A. (1994). Nitrogen-fixing stem nodules of the Legume, Discolobium pulchellum Benth. The New Phytologist, 128(2), 283–295. https://doi.org/10.1111/j.1469-8137.1994.tb04012.x
Pawlowski, K., & Sprent, J. I. (2008). Comparison Between Actinorhizal And Legume Symbiosis. In K. Pawlowski & W. E. Newton (Eds.), Nitrogen-fixing Actinorhizal Symbioses (pp. 261–288). Springer Netherlands. https://doi.org/10.1007/978-1-4020-3547-0_10
Soltis, D. E., Soltis, P. S., Morgan, D. R., Swensen, S. M., Mullin, B. C., Dowd, J. M., & Martin, P. G. (1995). Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences of the United States of America, 92(7), 2647–2651.
Sprent, J. I. (2008). Evolution and Diversity of Legume Symbiosis. In M. J. Dilworth, E. K. James, J. I. Sprent, & W. E. Newton (Eds.), Nitrogen-fixing Leguminous Symbioses (pp. 1–21). Springer Netherlands. https://doi.org/10.1007/978-1-4020-3548-7_1
Tedersoo, L., Laanisto, L., Rahimlou, S., Toussaint, A., Hallikma, T., & Pärtel, M. (2018). Global database of plants with root-symbiotic nitrogen fixation: NodDB. Journal of Vegetation Science, 29(3), 560–568. https://doi.org/10.1111/jvs.12627

Taxon origin

Origin in Europe: Native

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Origin in Europe
Origin in Europe was assessed according to the geographic origin of the species. Native taxa are plants that are native to at least part of Europe, although some of them are nowadays alien in other European regions. Species introduced intentionally or unintentionally by humans to Europe from other continents are alien (non-native) plants. We distinguished two categories of alien plants according to their residence time. Archaeophytes are plants introduced to Europe until the Middle Ages, while neophytes are plants introduced after 1500 AD. Data were compiled from Pyšek et al. (2012), GloNAF database (van Kleunen et al 2019), Verloove (2019), Euro+Med database (2021), POWO database (POWO 2021), complemented by additional sources such as national and regional floras.

Categories

Native

Archeophyte

Neophyte

Data source and citation

Axmanová, I. (2022). Origin in Europe. – www.FloraVeg.EU.

Further references

van Kleunen, M., Pyšek, P., Dawson, W., Essl, F., Kreft, H., Pergl, J. et al. (2019). The Global Naturalized Alien Floras (GloNAF) database. Ecology, 100(1):e02542. https://doi.org/10.1002/ecy.2542
Euro+Med (2021). Euro+Med PlantBase – the information resource for Euro-Mediterranean plant diversity. Available at http://ww2.bgbm.org/EuroPlusMed/query.asp [accessed May 2021]
POWO (2021). Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. Available at http://www.plantsoftheworldonline.org/ [accessed May 2021]
Pyšek P., Danihelka J., Sádlo J., Chrtek J. Jr., Chytrý M., … Tichý L. (2012) Catalogue of alien plants of the Czech Republic (2nd edition): checklist update, taxonomic diversity and invasion patterns. Preslia 84(2), 155–255.
Verloove, F. (2019). Manual of the Alien Plants of Belgium. Available at http://alienplantsbelgium.be/ [accessed May 2019]

Ecology

Environmental relationships

Substrate humidity relationship: Mesic

Ellenberg-type indicator values

Moisture indicator value: 6

Habitat and sociology

Syntaxon

Diagnostic species of phytosociological classes: MF (JUN) Juncetea maritimi

EUNIS habitat

Diagnostic species of EUNIS habitats: MA211 Arctic coastal saltmarsh

Broad habitat

Occurrence in broad habitats: Coastal saltmarsh

Distribution

Country-based map: Euro+Med Plantbase

No subordinate taxa were found for this item.

Primula nutans

Data

Trophic mode

Taxon origin

Ecology

Environmental relationships

Ellenberg-type indicator values

Habitat and sociology

Syntaxon

EUNIS habitat

Broad habitat

Distribution